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The airport was officially opened in December 1963.[3] It replaced Polje Airport in the former Municipality of Polje near Ljubljana,[4] which served as the city's airport from 1933 and was Slovenia's first civil airport.[5] Regular flights from the new airport at Brnik began in January 1964.[3]

On December 8, 2004, the airport received its first annual millionth passenger. Overall, the airport handled 1,321,100 passengers in 2013, representing a 10.2% rise in traffic figures compared to the previous year. It is currently the only airport in Slovenia with scheduled air traffic.

Due to growing air traffic and Slovenia's EU entry, which requires the separation of traffic into Schengen and non-Schengen, Aerodrom Ljubljana Airport Authorities have prepared a redevelopment plan for the passenger terminal with emphasis on expanding passenger capacity in the mid- to long-term time frame. The terminal expansion will be concluded in two phases. Works on the first phase began in early July 2007 to accommodate Slovenia's entry into the Schengen Area in December 2007. The terminal building (T1) was extended with a new upper level added to it and completely renovated; the floor that was added on top of the departure lounge added an additional 4,000 m2 (43,000 sq ft), and four jetways have also been installed so that passengers have easier access to the terminal and aircraft. A walkway to the second terminal building (T2) will be added after the T2 terminal is approved. With completion of the work on T1, the airport gained extra floor area, which in the short term will ensure the separation of Schengen and non-Schengen traffic.

The runway of Ljubljana Jože Pučnik Airport was closed to air traffic in April 2010 during which time, the entire length of the asphalt surface of the runway was renovated, as well as the asphalt surface on some parts of the taxiways.

The second phase of the expansion,[6] which had been planned to begin in 2013, but was postponed indefinitely by minority shareholders of Aerodrom Ljubljana,[7] includes the construction of a completely new airport terminal (T2). It will be built right next to the old one (T1), using the existing infrastructure as a connecting walkway. The new terminal building (T2) will expand over 32,000 m2 (340,000 sq ft), where 40 check-in counters will be set up (including some automatic ones) and the installation of three baggage carousels is planned for luggage claim. It will also offer 8 jetways for direct entry from the terminal to the aircraft. There will be room in the terminal for airlines, travel agencies, restaurants and shops, and there are also plans for business lounges and additional services for passengers. The capacity of T2 will be 2.5 million passengers annually (850 departing and 850 arriving passengers per hour). T2 will only be used for Schengen traffic, and non-Schengen traffic will flow through the new part of the old terminal (T1). This will create some redundant space in T1, which will be converted for commercial purposes. The opening of T2 was originally planned for May 2015 but the new date is currently unknown.[8]

To the north, a business and logistics center named Aeropolis Ljubljana[9] is planned to be built by 2020. It will consist of four parts: a business center, business park, logistic center, and hotel-conference complex. Other major projects include relocation of the road from Kranj to Mengeš to the north and a new train station, which will connect the airport and its logistics center with surrounding cities.[10]

The airport is served by an exit off the A2 motorway and by bus service connecting it with Ljubljana and Kranj. There is also a bus connection between Ljubljana Airport and Klagenfurt Airport in Austria.